Heterogeneity Governs 3D‐Cultures of Clinically Relevant Microbial Communities

Author:

Peneda Pacheco Daniela1ORCID,Bertoglio Federico23ORCID,Butnarasu Cosmin4ORCID,Suarez Vargas Natalia1ORCID,Guagliano Giuseppe1ORCID,Ziccarelli Anna1ORCID,Briatico‐Vangosa Francesco1ORCID,Ruzzi Vincenzo1ORCID,Buzzaccaro Stefano1ORCID,Piazza Roberto1ORCID,van Uden Sebastião1ORCID,Crotti Elena5ORCID,Visentin Sonja4ORCID,Visai Livia26ORCID,Petrini Paola1ORCID

Affiliation:

1. Department of Chemistry Materials and Chemical Engineering “Giulio Natta” Politecnico di Milano Piazza Leonardo da Vinci, 32 20133 Milan Italy

2. Molecular Medicine Department (DMM) Center for Health Technologies (CHT) UdR INSTM University of Pavia Viale Taramelli 3/B 27100 Pavia Italy

3. School of Advanced Studies IUSS Pavia Piazza della Vittoria, 15 27100 Pavia Italy

4. Molecular Biotechnology and Health Sciences Department University of Turin Via Nizza 52 10126 Turin Italy

5. Department of Food Environmental and Nutritional Sciences (DeFENS) University of Milan Via Celoria 2 Milan 20133 Italy

6. Medicina Clinica‐Specialistica UOR5 Laboratorio di Nanotecnologie ICS Maugeri IRCCS Via S. Boezio 28 Pavia 27100 Italy

Abstract

AbstractThe intrinsic heterogeneity of bacterial niches should be retained in in vitro cultures to represent the complex microbial ecology. As a case study, mucin‐containing hydrogels ‐CF‐Mu3Gel ‐ are generated by diffusion‐induced gelation, bioinspired on cystic fibrosis (CF) mucus, and a microbial niche challenging current therapeutic strategies. At breathing frequency, CF‐Mu3Gel exhibits a G′ and G″ equal to 24 and 3.2 Pa, respectively. Notably, CF‐Mu3Gel exhibits structural gradients with a gradual reduction of oxygen tension across its thickness (280–194 µmol L−1). Over the culture period, a steep decline in oxygen concentration occurs just a few millimeters below the air–mucus interface in CF‐Mu3Gel, similar to those of CF airway mucus. Importantly, the distinctive features of CF‐Mu3Gel significantly influence bacterial organization and antimicrobial tolerance in mono‐ and co‐cultures of Staphylococcus aureus and Pseudomonas aeruginosa that standard cultures are unable to emulate. The antimicrobial susceptibility determined in CF‐Mu3Gel corroborates the mismatch on the efficacy of antimicrobial treatment between planktonically cultured bacteria and those in patients. With this example‐based research, new light is shed on the understanding of how the substrate influences microbial behavior, paving the way for improved fundamental microbiology studies and more effective drug testing and development.

Publisher

Wiley

Subject

Electrochemistry,Condensed Matter Physics,Biomaterials,Electronic, Optical and Magnetic Materials

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